Novel 5-lipoxygenase isoforms affect the biosynthesis of 5-lipoxygenase products

FASEB Journal

Volumn 25, Issue 3, 2011, Pages 1097-1105

  Boudreau, Luc H ^a,b   Bertin, Jonathan ^a   Robichaud, Philippe P ^a   Laflamme, Mark ^c,d   Ouellette, Rodney J ^c   Flamand, Nicolas ^b   Surette, Marc E ^a  

^a UNIVERSITÉ DE MONCTON   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c ATLANTIC CANCER RESEARCH INSTITUTE   (Canada)

^d FISHERIES AND OCEANS CANADA   (Canada)

Author keywords

Eicosanoids; Inflammation; Leukocytes; Leukotrienes; Lipid mediators

Indexed keywords

ARACHIDONATE 5 LIPOXYGENASE;

ARTICLE; BIOSYNTHESIS; EXON; HUMAN; HUMAN CELL; LEUKOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 79954573836     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-173856     Document Type: Article

References (51)

1. Leff, J. A., Busse, W. W., Pearlman, D., Bronsky, E. A., Kemp, J., Hendeles, L., Dockhorn, R., Kundu, S., Zhang, J., Seidenberg, B. C., and Reiss, T. F. (1998) Montelukast, a leukotrienereceptor antagonist, for the treatment of mild asthma and exercise-induced bronchoconstriction. N. Engl. J. Med. 339, 147-152 (Pubitemid 28328478)
2. Peters-Golden, M., and Henderson, W. R., Jr. (2007) Leukotrienes. N. Engl. J. Med. 357, 1841-1854
3. Flamand, N., Mancuso, P., Serezani, C. H., and Brock, T. G. (2007) Leukotrienes: mediators that have been typecast as villains. Cell. Mol. Life Sci. 64, 2657-2670 (Pubitemid 350035614)
4. Tardif, J. C., L'Allier P. L., Ibrahim, R., Gregoire, J. C., Nozza, A., Cossette, M., Kouz, S., Lavoie, M. A., Paquin, J., Brotz, T. M., Taub, R., and Pressacco, J. Treatment with 5-lipoxygenase inhibitor VIA-2291 (Atreleuton) in patients with recent acute coronary syndrome. Circ. Cardiovasc Imaging 3, 298-307
5. Helgadottir, A., Manolescu, A., Thorleifsson, G., Gretarsdottir, S., Jonsdottir, H., Thorsteinsdottir, U., Samani, N. J., Gudmundsson, G., Grant, S. F., Thorgeirsson, G., Sveinbjornsdottir, S., Valdimarsson, E. M., Matthiasson, S. E., Johannsson, H., Gudmundsdottir, O., Gurney, M. E., Sainz, J., Thorhallsdottir, M., Andresdottir, M., Frigge, M. L., Topol, E. J., Kong, A., Gudnason, V., Hakonarson, H., Gulcher, J. R., and Stefansson, K. (2004) The gene encoding 5-lipoxygenase activating protein confers risk of myocardial infarction and stroke. Nat. Genet. 36, 233-239 (Pubitemid 38282747)
6. Dwyer, J. H., Allayee, H., Dwyer, K. M., Fan, J., Wu, H., Mar, R., Lusis, A. J., and Mehrabian, M. (2004) Arachidonate 5-lipoxygenase promoter genotype, dietary arachidonic acid, and atherosclerosis. N. Engl. J. Med. 350, 29-37 (Pubitemid 38032181)
7. Finkensieper, A., Kieser, S., Bekhite, M. M., Richter, M., Mueller, J. P., Graebner, R., Figulla, H. R., Sauer, H., and Wartenberg, M. (2010) The 5-lipoxygenase pathway regulates vasculogenesis in differentiating mouse embryonic stem cells. Cardiovasc. Res. 86, 37-44
8. Chen, Y., Li, D., and Li, S. (2009) The Alox5 gene is a novel therapeutic target in cancer stem cells of chronic myeloid leukemia. Cell Cycle 8, 3488-3492
9. Borgeat, P., Hamberg, M., and Samuelsson, B. (1976) Transformation of arachidonic acid and homo-gamma-linolenic acid by rabbit polymorphonuclear leukocytes. Monohydroxy acids from novel lipoxygenases. J. Biol. Chem. 251, 7816-7820 (Pubitemid 8015793)
10. Serhan, C. N. Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am. J Pathol. 177, 1576-1591
11. Brock, T. G., McNish, R. W., and Peters-Golden, M. (1995) Translocation and leukotriene synthetic capacity of nuclear 5-lipoxygenase in rat basophilic leukemia cells and alveolar macrophages. J. Biol. Chem. 270, 21652-21658
12. Rouzer, C. A., and Samuelsson, B. (1987) Reversible, calciumdependent membrane association of human leukocyte 5-lipoxygenase. Proc. Natl. Acad. Sci. U. S. A. 84, 7393-7397 (Pubitemid 18035710)
13. Woods, J. W., Evans, J. F., Ethier, D., Scott, S., Vickers, P. J., Hearn, L., Heibein, J. A., Charleson, S., and Singer, I. I. (1993) 5-lipoxygenase and 5-lipoxygenase-activating protein are localized in the nuclear envelope of activated human leukocytes. J. Exp. Med. 178, 1935-1946 (Pubitemid 23344852)
14. Allard, J. B., and Brock, T. G. (2005) Structural organization of the regulatory domain of human 5-lipoxygenase. Curr. Protein Pept. Sci. 6, 125-131 (Pubitemid 40614136)
15. Chen, X. S., and Funk, C. D. (2001) The N-terminal "betabarrel" domain of 5-lipoxygenase is essential for nuclear membrane translocation. J. Biol. Chem. 276, 811-818 (Pubitemid 32050382)
16. Hammarberg, T., Provost, P., Persson, B., and Radmark, O. (2000) The N-terminal domain of 5-lipoxygenase binds calcium and mediates calcium stimulation of enzyme activity. J. Biol. Chem. 275, 38787-38793 (Pubitemid 32009215)
17. Provost, P., Doucet, J., Hammarberg, T., Gerisch, G., Samuelsson, B., and Radmark, O. (2001) 5-Lipoxygenase interacts with coactosin-like protein. J. Biol. Chem. 276, 16520-16527
18. Rakonjac, M., Fischer, L., Provost, P., Werz, O., Steinhilber, D., Samuelsson, B., and Radmark, O. (2006) Coactosin-like protein supports 5-lipoxygenase enzyme activity and up-regulates leukotriene A4 production. Proc. Natl. Acad. Sci. U. S. A. 103, 13150-13155 (Pubitemid 44338931)
19. Abramovitz, M., Wong, E., Cox, M. E., Richardson, C. D., Li, C., and Vickers, P. J. (1993) 5-lipoxygenase-activating protein stimulates the utilization of arachidonic acid by 5-lipoxygenase. Eur. J. Biochem. 215, 105-111 (Pubitemid 23211131)
20. Flamand, N., Lefebvre, J., Surette, M. E., Picard, S., and Borgeat, P. (2006) Arachidonic acid regulates the translocation of 5-lipoxygenase to the nuclear membranes in human neutrophils. J. Biol. Chem. 281, 129-136 (Pubitemid 43671171)
21. Radmark, O., Werz, O., Steinhilber, D., and Samuelsson, B. (2007) 5-Lipoxygenase: regulation of expression and enzyme activity. Trends Biochem. Sci. 32, 332-341 (Pubitemid 47021417)
22. Newcomer, M. E., and Gilbert, N. C. (2010) Location, location, location: compartmentalization of early events in leukotriene biosynthesis. J. Biol. Chem. 13, 25109-25114
23. Funk, C. D., Hoshiko, S., Matsumoto, T., Rdmark, O., and Samuelsson, B. (1989) Characterization of the human 5-lipoxygenase gene. Proc. Natl. Acad. Sci. U. S. A. 86, 2587-2591 (Pubitemid 19112592)
24. Hoshiko, S., Radmark, O., and Samuelsson, B. (1990) Characterization of the human 5-lipoxygenase gene promoter. Proc. Natl. Acad. Sci. U. S. A. 87, 9073-9077 (Pubitemid 120030567)
25. Dishart, D., Schnur, N., Klan, N., Werz, O., Steinhilber, D., Samuelsson, B., and Radmark, O. (2005) GC-rich sequences in the 5-lipoxygenase gene promoter are required for expression in Mono Mac 6 cells, characterization of a novel Sp1 binding site. Biochim. Biophys. Acta 1738, 37-47 (Pubitemid 43124108)
26. Sorg, B. L., Klan, N., Seuter, S., Dishart, D., Radmark, O., Habenicht, A., Carlberg, C., Werz, O., and Steinhilber, D. (2006) Analysis of the 5-lipoxygenase promoter and characterization of a vitamin D receptor binding site. Biochim. Biophys. Acta 1761, 686-697 (Pubitemid 44164374)
27. Seuter, S., Sorg, B. L., and Steinhilber, D. (2006) The coding sequence mediates induction of 5-lipoxygenase expression by Smads3/4. Biochem. Biophys. Res. Commun. 348, 1403-1410 (Pubitemid 44291354)
28. Seuter, S., Vaisanen, S., Radmark, O., Carlberg, C., and Steinhilber, D. (2007) Functional characterization of vitamin D responding regions in the human 5-lipoxygenase gene. Biochim. Biophys. Acta 1771, 864-872 (Pubitemid 46900904)
29. Uhl, J., Klan, N., Rose, M., Entian, K. D., Werz, O., and Steinhilber, D. (2002) The 5-lipoxygenase promoter is regulated by DNA methylation. J. Biol. Chem. 277, 4374-4379 (Pubitemid 34975655)
30. Johnson, J. M., Castle, J., Garrett-Engele, P., Kan, Z., Loerch, P. M., Armour, C. D., Santos, R., Schadt, E. E., Stoughton, R., and Shoemaker, D. D. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302, 2141-2144 (Pubitemid 38017950)
31. Ben-Dov, C., Hartmann, B., Lundgren, J., and Valcarcel, J. (2008) Genome-wide analysis of alternative pre-mRNA splicing. J. Biol. Chem. 283, 1229-1233
32. Roos, K. L., and Simmons, D. L. (2005) Cyclooxygenase variants: the role of alternative splicing. Biochem. Biophys. Res. Commun. 338, 62-69 (Pubitemid 41540537)
33. Kilty, I., Logan, A., and Vickers, P. J. (1999) Differential characteristics of human 15-lipoxygenase isozymes and a novel splice variant of 15S-lipoxygenase. Eur. J. Biochem. 266, 83-93
34. Jendraschak, E., Kaminski, W. E., Kiefl, R., and von Schacky, C. (1996) The human leukotriene A4 hydrolase gene is expressed in two alternatively spliced mRNA forms. Biochem. J. 314, 733-737
35. Boyum, A. (1968) Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand. J. Clin. Lab. Invest. Suppl. 97, 77-89
36. Flamand, N., Surette, M. E., Picard, S., Bourgoin, S., and Borgeat, P. (2002) Cyclic AMP-mediated inhibition of 5-lipoxygenase translocation and leukotriene biosynthesis in human neutrophils. Mol. Pharmacol. 62, 250-256 (Pubitemid 34804103)
37. Werz, O., Szellas, D., and Steinhilber, D. (2000) Reactive oxygen species released from granulocytes stimulate 5-lipoxygenase activity in a B-lymphocytic cell line. Eur. J. Biochem. 267, 1263-1269 (Pubitemid 30143263)
38. Ring, W. L., Riddick, C. A., Baker, J. R., Glass, C. K., and Bigby, T. D. (1997) Activated lymphocytes increase expression of 5-lipoxygenase and its activating protein in THP-1 cells. Am. J. Physiol. Cell. Physiol. 273, C2057-C2064
39. Borgeat, P., Picard, S., Vallerand, P., Bourgoin, S., Odeimat, A., Sirois, P., and Poubelle, P. E. (1990) Automated on-line extraction and profiling of lipoxygenase products of arachidonic acid by high-performance liquid chromatography. Methods Enzymol. 187, 98-116 (Pubitemid 20309273)
40. Markwell, M. A., Haas, S. M., Tolbert, N. E., and Bieber, L. L. (1981) Protein determination in membrane and lipoprotein samples: manual and automated procedures. Methods Enzymol. 72, 296-303
41. Werz, O., Tretiakova, I., Michel, A., Ulke-Lemee, A., Hornig, M., Franke, L., Schneider, G., Samuelsson, B., Radmark, O., and Steinhilber, D. (2005) Caspase-mediated degradation of human 5-lipoxygenase in B lymphocytic cells. Proc. Natl. Acad. Sci. U. S. A. 102, 13164-13169 (Pubitemid 41324996)
42. Flamand, N., Luo, M., Peters-Golden, M., and Brock, T. G. (2009) Phosphorylation of serine 271 on 5-lipoxygenase and its role in nuclear export. J. Biol. Chem. 284, 306-313
43. Arseneau, J. R., Laflamme, M., Lewis, S. M., Maicas, E., and Ouellette, R. J. (2009) Multiple isoforms of PAX5 are expressed in both lymphomas and normal B-cells. Br. J. Haematol. 147, 328-338
44. Keren, H., Lev-Maor, G., and Ast, G. (2010) Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet. 11, 345-355
45. Matlin, A. J., Clark, F., and Smith, C. W. (2005) Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell. Biol. 6, 386-398 (Pubitemid 40637856)
46. Gao, K., Masuda, A., Matsuura, T., and Ohno, K. (2008) Human branch point consensus sequence is yUnAy. Nucleic Acids Res. 36, 2257-2267 (Pubitemid 351575093)
47. Michel, A. A., Steinhilber, D., and Werz, O. (2008) Development of a method for expression and purification of the regulatory C2-like domain of human 5-lipoxygenase. Protein Expr. Purif. 59, 110-116
48. Hemak, J., Gale, D., and Brock, T. G. (2002) Structural characterization of the catalytic domain of the human 5-lipoxygenase enzyme. J. Mol. Model. 8, 102-112 (Pubitemid 36153516)
49. Hegg, E. L., and Que, L., Jr. (1997) The 2-His-1-carboxylate facial triad-an emerging structural motif in mononuclear nonheme iron (II) enzymes. Eur. J. Biochem. 250, 625-629 (Pubitemid 28022477)
50. Plante, H., Picard, S., Mancini, J., and Borgeat, P. (2006) 5-Lipoxygenase-activating protein homodimer in human neutrophils: evidence for a role in leukotriene biosynthesis. Biochem. J. 393, 211-218 (Pubitemid 43049317)
51. Ferguson, A. D., McKeever, B. M., Xu, S., Wisniewski, D., Miller, D. K., Yamin, T. T., Spencer, R. H., Chu, L., Ujjainwalla, F., Cunningham, B. R., Evans, J. F., and Becker, J. W. (2007) Crystal structure of inhibitor-bound human 5-lipoxygenase-activating protein. Science 317, 510-512 (Pubitemid 47196114)